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Journal of Immunology Research
Volume 2014, Article ID 591489, 11 pages
http://dx.doi.org/10.1155/2014/591489
Review Article

The Many Faces of Human Leukocyte Antigen-G: Relevance to the Fate of Pregnancy

Department of Clinical Biochemistry, Centre for Immune Regulation and Reproductive Immunology (CIRRI), Copenhagen University Hospital (Roskilde) and Roskilde Hospital, 7-13 Køgevej, 4000 Roskilde, Denmark

Received 9 December 2013; Accepted 17 January 2014; Published 4 March 2014

Academic Editor: Roberta Rizzo

Copyright © 2014 Mette Dahl et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Ishitani and D. E. Geraghty, “Alternative splicing of HLA-G transcripts yields proteins with primary structures resembling both class I and class II antigens,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 9, pp. 3947–3951, 1992. View at Google Scholar · View at Scopus
  2. S. A. Ellis, I. L. Sargent, C. W. G. Redman, and A. J. McMichael, “Evidence for a novel HLA antigen found on human extravillous trophoblast and a choriocarcinoma cell line,” Immunology, vol. 59, no. 4, pp. 595–601, 1986. View at Google Scholar · View at Scopus
  3. P. Paul, F. A. Cabestre, E. C. Ibrahim et al., “Identification of HLA-G7 as a new splice variant of the HLA-G mRNA and expression of soluble HLA-G5, -G6, and -G7 transcripts in human transfected cells,” Human Immunology, vol. 61, no. 11, pp. 1138–1149, 2000. View at Publisher · View at Google Scholar · View at Scopus
  4. R. Apps, L. Gardner, A. M. Sharkey, N. Holmes, and A. Moffett, “A homodimeric complex of HLA-G on normal trophoblast cells modulates antigen-presenting cells via LILRB1,” European Journal of Immunology, vol. 37, no. 7, pp. 1924–1937, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Gonen-Gross, H. Achdout, T. I. Arnon et al., “The CD85J/leukocyte inhibitory receptor-1 distinguishes between conformed and β2-microglobulin-free HLA-G molecules,” Journal of Immunology, vol. 175, no. 8, pp. 4866–4874, 2005. View at Google Scholar · View at Scopus
  6. P. J. Morales, J. L. Pace, J. S. Platt, D. K. Langat, and J. S. Hunt, “Synthesis of β2-microglobulin-free, disulphide-linked HLA-G5 homodimers in human placental villous cytotrophoblast cells,” Immunology, vol. 122, no. 2, pp. 179–188, 2007. View at Publisher · View at Google Scholar · View at Scopus
  7. T. V. F. Hviid, O. B. Christiansen, J. K. Johansen et al., “Characterization of a new HLA-G allele encoding a nonconservative amino acid substitution in the α3 domain (exon 4) and its relevance to certain complications in pregnancy,” Immunogenetics, vol. 53, no. 1, pp. 48–53, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. T. V. F. Hviid, “HLA-G in human reproduction: aspects of genetics, function and pregnancy complications,” Human Reproduction Update, vol. 12, no. 3, pp. 209–232, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Dahl and T. V. F. Hviid, “Human leucocyte antigen class Ib molecules in pregnancy success and early pregnancy loss,” Human Reproduction Update, vol. 18, no. 1, pp. 92–109, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. S. A. Ellis, M. S. Palmer, and A. J. McMichael, “Human trophoblast and the choriocarcinoma cell line BeWo express a truncated HLA class I molecule,” Journal of Immunology, vol. 144, no. 2, pp. 731–735, 1990. View at Google Scholar · View at Scopus
  11. A. Ishitani, N. Sageshima, N. Lee et al., “Protein expression and peptide binding suggest unique and interacting functional roles for HLA-E, F, and G in maternal-placental immune recognition,” Journal of Immunology, vol. 171, no. 3, pp. 1376–1384, 2003. View at Google Scholar · View at Scopus
  12. P. J. Morales, J. L. Pace, J. S. Platt et al., “Placental cell expression of HLA-G2 isoforms is limited to the invasive trophoblast phenotype,” Journal of Immunology, vol. 171, no. 11, pp. 6215–6224, 2003. View at Google Scholar · View at Scopus
  13. C. Solier, M. Aguerre-Girr, F. Lenfant et al., “Secretion of pro-apoptotic intron 4-retaining soluble HLA-G1 by human villous trophoblast,” European Journal of Immunology, vol. 32, no. 12, pp. 3576–3586, 2002. View at Google Scholar
  14. B. Fuzzi, R. Rizzo, L. Criscuoli et al., “HLA-G expression in early embryos is a fundamental prerequisite for the obtainment of pregnancy,” European Journal of Immunology, vol. 32, no. 2, pp. 311–315, 2002. View at Google Scholar
  15. J. S. Hunt, L. Jadhav, W. Chu, D. E. Geraghty, and C. Ober, “Soluble HLA-G circulates in maternal blood during pregnancy,” The American Journal of Obstetrics and Gynecology, vol. 183, no. 3, pp. 682–688, 2000. View at Publisher · View at Google Scholar · View at Scopus
  16. M. H. Larsen, M. Bzorek, M. B. Pass et al., “Human leukocyte antigen-G in the male reproductive system and in seminal plasma,” Molecular Human Reproduction, vol. 17, no. 12, pp. 727–738, 2011. View at Publisher · View at Google Scholar · View at Scopus
  17. D. K. Langat, J. Sue Platt, O. Tawfik, A. T. Fazleabas, and J. S. Hunt, “Differential expression of human leukocyte antigen-G (HLA-G) messenger RNAs and proteins in normal human prostate and prostatic adenocarcinoma,” Journal of Reproductive Immunology, vol. 71, no. 1, pp. 75–86, 2006. View at Publisher · View at Google Scholar · View at Scopus
  18. R. Rizzo, B. Fuzzi, M. Stignani et al., “Soluble HLA-G molecules in follicular fluid: a tool for oocyte selection in IVF?” Journal of Reproductive Immunology, vol. 74, no. 1-2, pp. 133–142, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. M. Colonna, F. Navarro, T. Bellón et al., “A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells,” Journal of Experimental Medicine, vol. 186, no. 11, pp. 1809–1818, 1997. View at Publisher · View at Google Scholar · View at Scopus
  20. M. Colonna, F. Navarro, and M. López-Botet, “A novel family of inhibitory receptors for HLA class I molecules that modulate function of lymphoid and myeloid cells,” Current Topics in Microbiology and Immunology, vol. 244, pp. 115–122, 1999. View at Google Scholar · View at Scopus
  21. S. Rajagopalan and E. O. Long, “A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells,” Journal of Experimental Medicine, vol. 189, no. 7, pp. 1093–1099, 1999. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Colonna, J. Samaridis, M. Cella et al., “Cutting edge: human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I-molecules,” Journal of Immunology, vol. 160, no. 7, pp. 3096–3100, 1998. View at Google Scholar · View at Scopus
  23. R. Rizzo, M. Vercammen, H. van de Velde, P. A. Horn, and V. Rebmann, “The importance of HLA-G expression in embryos, trophoblast cells, and embryonic stem cells,” Cellular and Molecular Life Sciences, vol. 68, no. 3, pp. 341–352, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. A. Gonzalez, V. Rebmann, J. LeMaoult, P. A. Horn, E. D. Carosella, and E. Alegre, “The immunosuppressive molecule HLA-G and its clinical implications,” Critical Reviews in Clinical Laboratory Sciences, vol. 49, no. 3, pp. 63–84, 2012. View at Google Scholar
  25. M. H. Larsen, S. Hylenius, A.-M. N. Andersen, and T. V. F. Hviid, “The 3′-untranslated region of the HLA-G gene in relation to pre-eclampsia: revisited,” Tissue Antigens, vol. 75, no. 3, pp. 253–261, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. D. E. Geraghty, B. H. Koller, and H. T. Orr, “A human major histocompatibility complex class I gene that encodes a protein with a shortened cytoplasmic segment,” Proceedings of the National Academy of Sciences of the United States of America, vol. 84, no. 24, pp. 9145–9149, 1987. View at Google Scholar · View at Scopus
  27. E. C. Castelli, C. T. Mendes-Junior, N. H. S. Deghaide et al., “The genetic structure of 3′untranslated region of the HLA-G gene: polymorphisms and haplotypes,” Genes and Immunity, vol. 11, no. 2, pp. 134–141, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. M. H. Larsen and T. V. F. Hviid, “Human leukocyte antigen-G polymorphism in relation to expression, function, and disease,” Human Immunology, vol. 70, no. 12, pp. 1026–1034, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Martelli-Palomino, J. A. Pancotto, Y. C. Muniz et al., “Polymorphic sites at the 3′ untranslated region of the HLA-G gene are associated with differential hla-g soluble levels in the Brazilian and French Population,” PLoS ONE, vol. 8, no. 10, Article ID e71742, 2013. View at Google Scholar
  30. T. V. F. Hviid, S. Hylenius, C. Rørbye, and L. G. Nielsen, “HLA-G allelic variants are associated with differences in the HLA-G mRNA isoform profile and HLA-G mRNA levels,” Immunogenetics, vol. 55, no. 2, pp. 63–79, 2003. View at Google Scholar · View at Scopus
  31. P. Rousseau, M. Le Discorde, G. Mouillot, C. Marcou, E. D. Carosella, and P. Moreau, “The 14 bp deletion-insertion polymorphism in the 3′ UT region of the HLA-G gene influences HLA-G mRNA stability,” Human Immunology, vol. 64, no. 11, pp. 1005–1010, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. S. G. Svendsen, B. M. Hantash, L. Zhao et al., “The expression and functional activity of membrane-bound human leukocyte antigen-G1 are influenced by the 3′-untranslated region,” Human Immunology, vol. 74, no. 7, pp. 818–827, 2013. View at Google Scholar
  33. C. W. G. Redman, A. J. McMichael, and G. M. Stirrat, “Class 1 major histocompatibility complex antigens on human extra-villous trophoblast,” Immunology, vol. 52, no. 3, pp. 457–468, 1984. View at Google Scholar · View at Scopus
  34. T. G. Wegmann, H. Lin, L. Guilbert, and T. R. Mosmann, “Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon?” Immunology Today, vol. 14, no. 7, pp. 353–356, 1993. View at Google Scholar · View at Scopus
  35. J. Trowsdale and A. Moffett, “NK receptor interactions with MHC class I molecules in pregnancy,” Seminars in Immunology, vol. 20, no. 6, pp. 317–320, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. A. King, C. Boocock, A. M. Sharkey et al., “Evidence for the expression of HLA-C class I mRNA and protein by human first trimester trophoblast,” Journal of Immunology, vol. 156, no. 6, pp. 2068–2076, 1996. View at Google Scholar · View at Scopus
  37. C. W. G. Redman, “Immunology of preeclampsia,” Seminars in Perinatology, vol. 15, no. 3, pp. 257–262, 1991. View at Google Scholar · View at Scopus
  38. S. Hylenius, A.-M. N. Andersen, M. Melbye, and T. V. F. Hviid, “Association between HLA-G genotype and risk of pre-eclampsia: a case-control study using family triads,” Molecular Human Reproduction, vol. 10, no. 4, pp. 237–246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. A. C. Iversen, O. T. D. Nguyen, L. F. Tømmerdal et al., “The HLA-G 14bp gene polymorphism and decidual HLA-G 14bp gene expression in pre-eclamptic and normal pregnancies,” Journal of Reproductive Immunology, vol. 78, no. 2, pp. 158–165, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. K. H. Lim, Y. Zhou, M. Janatpour et al., “Human cytotrophoblast differentiation/invasion is abnormal in pre- eclampsia,” The American Journal of Pathology, vol. 151, no. 6, pp. 1809–1818, 1997. View at Google Scholar · View at Scopus
  41. M. O'Brien, T. McCarthy, D. Jenkins et al., “Altered HLA-G transcription in pre-eclampsia is associated with allele specific inheritance: possible role of the HLA-G gene in susceptibility to the disease,” Cellular and Molecular Life Sciences, vol. 58, no. 12-13, pp. 1943–1949, 2001. View at Google Scholar · View at Scopus
  42. G. A. Harrison, K. E. Humphrey, I. B. Jakobsen, and D. W. Cooper, “A 14 bp deletion polymorphism in the HLA-G gene,” Human Molecular Genetics, vol. 2, no. 12, p. 2200, 1993. View at Google Scholar · View at Scopus
  43. N. Hara, T. Fujii, T. Yamashita, S. Kozuma, T. Okai, and Y. Taketani, “Altered expression of human leukocyte antigen G, (HLA-G) on extravillous trophoblasts in preeclampsia: immunohistological demonstration with anti-HLA-G specific antibody, “87G” and anti-cytokeratin antibody, ‘CAM5. 2’,” The American Journal of Reproductive Immunology, vol. 36, no. 6, pp. 349–358, 1996. View at Google Scholar · View at Scopus
  44. D. S. Goldman-Wohl, I. Ariel, C. Greenfield, J. Hanoch, and S. Yagel, “HLA-G expression in extravillous trophoblasts is an intrinsic property of cell differentiation: a lesson learned from ectopic pregnancies,” Molecular Human Reproduction, vol. 6, no. 6, pp. 535–540, 2000. View at Google Scholar · View at Scopus
  45. P. Moreau, L. Contu, F. Alba et al., “HLA-G gene polymorphism in human placentas: possible association of G*0106 allele with preeclampsia and miscarriage,” Biology of Reproduction, vol. 79, no. 3, pp. 459–467, 2008. View at Publisher · View at Google Scholar · View at Scopus
  46. Z. Zhang, Y. Li, L. L. Zhang, L. T. Jia, and X. Q. Yang, “Association of 14 bp insertion/deletion polymorphism of the HLA-G gene in father with severe preeclampsia in Chinese,” Tissue Antigens, vol. 80, no. 2, pp. 158–164, 2012. View at Google Scholar
  47. T. V. F. Hviid, R. Rizzo, L. Melchiorri, M. Stignani, and O. R. Baricordi, “Polymorphism in the 5′ upstream regulatory and 3′ untranslated regions of the HLA-G gene in relation to soluble HLA-G and IL-10 expression,” Human Immunology, vol. 67, no. 1-2, pp. 53–62, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. R. Rizzo, T. V. F. Hviid, M. Govoni et al., “HLA-G genotype and HLA-G expression in systemic lupus erythematosus: HLA-G as a putative susceptibility gene in systemic lupus erythematosus,” Tissue Antigens, vol. 71, no. 6, pp. 520–529, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Twito, J. Joseph, A. Mociornita, V. Rao, H. Ross, and D. H. Delgado, “The 14-bp deletion in the HLA-G gene indicates a low risk for acute cellular rejection in heart transplant recipients,” Journal of Heart and Lung Transplantation, vol. 30, no. 7, pp. 778–782, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. X. Y. Chen, W. H. Yan, A. Lin, H. H. Xu, J. G. Zhang, and X. X. Wang, “The 14 bp deletion polymorphisms in HLA-G gene play an important role in the expression of soluble HLA-G in plasma,” Tissue Antigens, vol. 72, no. 4, pp. 335–341, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. F. X. Wu, L. J. Wu, X. Y. Luo et al., “Lack of association between HLA-G 14-bp polymorphism and systemic lupus erythematosus in a Han Chinese population,” Lupus, vol. 18, no. 14, pp. 1259–1266, 2009. View at Google Scholar · View at Scopus
  52. X. Q. Zheng, C. C. Li, D. P. Xu et al., “Analysis of the plasma soluble human leukocyte antigen-G and interleukin-10 levels in childhood atopic asthma,” Human Immunology, vol. 71, no. 10, pp. 982–987, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Rizzo, A. S. Andersen, M. R. Lassen et al., “Soluble Human Leukocyte Antigen-G isoforms in maternal plasma in early and late pregnancy,” The American Journal of Reproductive Immunology, vol. 62, no. 5, pp. 320–338, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. P. M. Emmer, I. Joosten, M. H. Schut, P. L. M. Zusterzeel, J. C. M. Hendriks, and E. A. P. Steegers, “Shift in expression of HLA-G mRNA spliceforms in pregnancies complicated by preeclampsia,” Journal of the Society for Gynecologic Investigation, vol. 11, no. 4, pp. 220–226, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. A. Gonzalez, E. Alegre, M. I. Torres et al., “Evaluation of HLA-G5 plasmatic levels during pregnancy and relationship with the 14-bp polymorphism,” The American journal of reproductive immunology, vol. 64, no. 5, pp. 367–374, 2010. View at Google Scholar · View at Scopus
  56. B. Riteau, N. Rouas-Freiss, C. Menier, P. Paul, J. Dausset, and E. D. Carosella, “HLA-G2, -G3, and -G4 isoforms expressed as nonmature cell surface glycoproteins inhibit NK and antigen-specific CTL cytolysis,” Journal of Immunology, vol. 166, no. 8, pp. 5018–5026, 2001. View at Google Scholar · View at Scopus
  57. J. LeMaoult, M. Daouya, J. Wu, M. Loustau, A. Horuzsko, and E. D. Carosella, “Synthetic HLA-G proteins for therapeutic use in transplantation,” The FASEB Journal, vol. 27, no. 9, pp. 3643–3651, 2013. View at Google Scholar
  58. D. A. Loisel, C. Billstrand, K. Murray et al., “The maternal HLA-G, 1597DeltaC null mutation is associated with increased risk of pre-eclampsia and reduced HLA-G expression during pregnancy in African-American women,” Molecular Human Reproduction, vol. 19, no. 3, pp. 144–152, 2013. View at Google Scholar
  59. Z. Tan, G. Randall, J. Fan et al., “Allele-specific targeting of microRNAs to HLA-G and risk of asthma,” The American Journal of Human Genetics, vol. 81, no. 4, pp. 829–834, 2007. View at Publisher · View at Google Scholar · View at Scopus
  60. S. M. Yie, L. H. Li, R. Xiao, and C. L. Librach, “A single base-pair mutation in the 3′-untranslated region of HLA-G mRNA is associated with pre-eclampsia,” Molecular Human Reproduction, vol. 14, no. 11, pp. 649–653, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. E. C. Castelli, P. Moreau, A. O. E. Chiromatzo et al., “In silico analysis of microRNAS targeting the HLA-G 3′ untranslated region alleles and haplotypes,” Human Immunology, vol. 70, no. 12, pp. 1020–1025, 2009. View at Publisher · View at Google Scholar · View at Scopus
  62. E. C. Castelli, C. T. Mendes-Junior, L. C. Veiga-Castelli, M. Roger, P. Moreau, and E. A. Donadi, “A comprehensive study of polymorphic sites along the HLA-G gene: implication for gene regulation and evolution,” Molecular Biology and Evolution, vol. 28, no. 11, pp. 3069–3086, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. J. di Cristofaro, D. El Moujally, A. Agnel et al., “HLA-G haplotype structure shows good conservation between different populations and good correlation with high, normal and low soluble HLA-G expression,” Human Immunology, vol. 74, no. 2, pp. 203–206, 2013. View at Google Scholar
  64. N. Rudstein-Svetlicky, R. Loewenthal, V. Horejsi, and E. Gazit, “HLA-G levels in serum and plasma,” Tissue Antigens, vol. 69, no. 1, pp. 140–142, 2007. View at Publisher · View at Google Scholar · View at Scopus
  65. T. V. F. Hviid, R. Rizzo, O. B. Christiansen, L. Melchiorri, A. Lindhard, and O. R. Baricordi, “HLA-G and IL-10 in serum in relation to HLA-G genotype and polymorphisms,” Immunogenetics, vol. 56, no. 3, pp. 135–141, 2004. View at Google Scholar · View at Scopus
  66. J. Nicodemus-Johnson, B. Laxman, R. K. Stern et al., “Maternal asthma and microRNA regulation of soluble HLA-G in the airway,” Journal of Allergy and Clinical Immunology, vol. 131, no. 6, pp. 1496–1503, 2013. View at Google Scholar
  67. E. A. Grzybowska, A. Wilczynska, and J. A. Siedlecki, “Breakthroughs and views: regulatory functions of 3′UTRs,” Biochemical and Biophysical Research Communications, vol. 288, no. 2, pp. 291–295, 2001. View at Publisher · View at Google Scholar · View at Scopus
  68. J. T. Mendell and H. C. Dietz, “When the message goes awry: disease-producing mutations that influence mRNA content and performance,” Cell, vol. 107, no. 4, pp. 411–414, 2001. View at Publisher · View at Google Scholar · View at Scopus
  69. V. Rebmann, M. Switala, I. Eue, and H. Grosse-Wilde, “Soluble HLA-G is an independent factor for the prediction of pregnancy outcome after ART: a German multi-centre study,” Human Reproduction, vol. 25, no. 7, pp. 1691–1698, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. M. J. Vercammen, A. Verloes, H. Van de Velde, and P. Haentjens, “Accuracy of soluble human leukocyte antigen-G for predicting pregnancy among women undergoing infertility treatment: meta-analysis,” Human Reproduction Update, vol. 14, no. 3, pp. 209–218, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. S. M. Yie, L. H. Li, Y. M. Li, and C. Librach, “HLA-G protein concentrations in maternal serum and placental tissue are decreased in preeclampsia,” The American Journal of Obstetrics and Gynecology, vol. 191, no. 2, pp. 525–529, 2004. View at Publisher · View at Google Scholar · View at Scopus
  72. K. Poláková, D. Kuba, and G. Russ, “The 4H84 monoclonal antibody detecting β2m free nonclassical HLA-G molecules also binds to free heavy chains of classical HLA class I antigens present on activated lymphocytes,” Human Immunology, vol. 65, no. 2, pp. 157–162, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Brusilovsky, M. Cordoba, B. Rosental et al., “Genome-wide siRNA screen reveals a new cellular partner of NK cell receptor KIR2DL4: heparan sulfate directly modulates KIR2DL4-mediated responses,” Journal of Immunology, vol. 191, no. 10, pp. 5256–5267, 2013. View at Google Scholar
  74. M. Ponte, C. Cantoni, R. Biassoni et al., “Inhibitory receptors sensing HLA-G1 molecules in pregnancy: decidua-associated natural killer cells express LIR-1 and CD94/NKG2A and acquire p49, an HLA-G1-specific receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 10, pp. 5674–5679, 1999. View at Google Scholar · View at Scopus
  75. Y.-R. Yu, X.-H. Tian, Y. Wang, and M.-F. Feng, “Rapid production of human KIR2DL4 extracellular domain and verification of its interaction with HLA-G,” Biochemistry, vol. 71, no. 1, pp. S60–S64, 2006. View at Publisher · View at Google Scholar · View at Scopus
  76. B. Riteau, C. Menier, I. Khalil-Daher et al., “HLA-G1 co-expression boosts the HLA class I-mediated NK lysis inhibition,” International Immunology, vol. 13, no. 2, pp. 193–201, 2001. View at Google Scholar · View at Scopus
  77. L. J. Chen, Z. Q. Han, H. Zhou, L. Zou, and P. Zou, “Inhibition of HLA-G expression via RNAi abolishes resistance of extravillous trophoblast cell line TEV-1 to NK lysis,” Placenta, vol. 31, no. 6, pp. 519–527, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. S. Rajagopalan, Y. T. Bryceson, S. P. Kuppusamy et al., “Activation of NK cells by an endocytosed receptor for soluble HLA-G,” PLoS Biology, vol. 4, no. 1, p. e9, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. N. Gömez-Lozano, R. de Pablo, S. Puente, and C. Vilches, “Recognition of HLA-G by the NK cell receptor KIR2DL4 is not essential for human reproduction,” European Journal of Immunology, vol. 33, no. 3, pp. 639–644, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. W. H. Yan, A. Lin, B. G. Chen et al., “Possible roles of KIR2DL4 expression on uNK cells in human pregnancy,” The American Journal of Reproductive Immunology, vol. 57, no. 4, pp. 233–242, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. G. M. Park, S. Lee, B. Park et al., “Soluble HLA-G generated by proteolytic shedding inhibits NK-mediated cell lysis,” Biochemical and Biophysical Research Communications, vol. 313, no. 3, pp. 606–611, 2004. View at Publisher · View at Google Scholar · View at Scopus
  82. W. Q. Zhang, D. P. Xu, D. Liu et al., “HLA-G1 and HLA-G5 isoforms have an additive effect on NK cytolysis,” Human Immunology, vol. 75, no. 2, pp. 182–189, 2013. View at Google Scholar
  83. L. Zhao, B. Purandare, J. Zhang, and B. M. Hantash, “beta2-Microglobulin-free HLA-G activates natural killer cells by increasing cytotoxicity and proinflammatory cytokine production,” Human Immunology, vol. 74, no. 4, pp. 417–424, 2013. View at Google Scholar
  84. A. van der Meer, H. G. M. Lukassen, B. van Cranenbroek et al., “Soluble HLA-G promotes Th1-type cytokine production by cytokine-activated uterine and peripheral natural killer cells,” Molecular Human Reproduction, vol. 13, no. 2, pp. 123–133, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. J. E. Cartwright and G. Balarajah, “Trophoblast interactions with endothelial cells are increased by interleukin-1β and tumour necrosis factor α and involve vascular cell adhesion molecule-1 and α4β1,” Experimental Cell Research, vol. 304, no. 1, pp. 328–336, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. Y. Guo, C. L. Lee, K. H. So et al., “Soluble human leukocyte antigen-g5 activates extracellular signal-regulated protein kinase signaling and stimulates trophoblast invasion,” PLoS ONE, vol. 8, no. 10, Article ID e76023, 2013. View at Google Scholar
  87. J. McCormick, G. S. J. Whitley, P. Le Bouteiller, and J. E. Cartwright, “Soluble HLA-G regulates motility and invasion of the trophoblast-derived cell line SGHPL-4,” Human Reproduction, vol. 24, no. 6, pp. 1339–1345, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. G. Amodio, A. Mugione, A. M. Sanchez et al., “HLA-G expressing DC-10 and CD4+ T cells accumulate in human decidua during pregnancy,” Human Immunology, vol. 74, no. 4, pp. 406–411, 2013. View at Google Scholar
  89. S. Gregori, D. Tomasoni, V. Pacciani et al., “Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL-10-dependent ILT4/HLA-G pathway,” Blood, vol. 116, no. 6, pp. 935–944, 2010. View at Google Scholar
  90. U. Feger, E. Tolosa, Y.-H. Huang et al., “HLA-G expression defines a novel regulatory T-cell subset present in human peripheral blood and sites of inflammation,” Blood, vol. 110, no. 2, pp. 568–577, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. Y. H. Huang, A. L. Zozulya, C. Weidenfeller, N. Schwab, and H. Wiendl, “T cell suppression by naturally occurring HLA-G-expressing regulatory CD4+ T cells is IL-10-dependent and reversible,” Journal of Leukocyte Biology, vol. 86, no. 2, pp. 273–281, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. A. Steinborn, T. Varkonyi, A. Scharf, F. Bahlmann, A. Klee, and C. Sohn, “Early detection of decreased soluble HLA-G levels in the maternal circulation predicts the occurrence of preeclampsia and intrauterine growth retardation during further course of pregnancy,” The American Journal of Reproductive Immunology, vol. 57, no. 4, pp. 277–286, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. S.-M. Yie, R. N. Taylor, and C. Librach, “Low plasma HLA-G protein concentrations in early gestation indicate the development of preeclampsia later in pregnancy,” The American Journal of Obstetrics and Gynecology, vol. 193, no. 1, pp. 204–208, 2005. View at Publisher · View at Google Scholar · View at Scopus
  94. R. Hackmon, A. Koifman, H. Hyobo, H. Glickman, E. Sheiner, and D. E. Geraghty, “Reduced third-trimester levels of soluble human leukocyte antigen G protein in severe preeclampsia,” The American Journal of Obstetrics and Gynecology, vol. 197, no. 3, pp. e251–e255, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. T. V. F. Hviid, L. G. Larsen, A. M. Hoegh, and M. Bzorek, “HLA-G expression in placenta in relation to HLA-G genotype and polymorphisms,” The American Journal of Reproductive Immunology, vol. 52, no. 3, pp. 212–217, 2004. View at Google Scholar · View at Scopus
  96. M. Coolman, M. de Maat, W. L. van Heerde et al., “Matrix Metalloproteinase-9 Gene -1562C/T Polymorphism Mitigates Preeclampsia,” Placenta, vol. 28, no. 7, pp. 709–713, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. V. Plaks, J. Rinkenberger, J. Dai et al., “Matrix metalloproteinase-9 deficiency phenocopies features of preeclampsia and intrauterine growth restriction,” Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 27, pp. 11109–11114, 2013. View at Google Scholar
  98. T. Tabata, S. McDonagh, H. Kawakatsu, and L. Pereira, “Cytotrophoblasts infected with a pathogenic human cytomegalovirus strain dysregulate cell-matrix and cell-cell adhesion molecules: a quantitative analysis,” Placenta, vol. 28, no. 5-6, pp. 527–537, 2007. View at Publisher · View at Google Scholar · View at Scopus
  99. B. Park, E. Spooner, B. L. Houser, J. L. Strominger, and H. L. Ploegh, “The HCMV membrane glycoprotein US10 selectively targets HLA-G for degradation,” Journal of Experimental Medicine, vol. 207, no. 9, pp. 2033–2041, 2010. View at Publisher · View at Google Scholar · View at Scopus
  100. M. Carreiras, S. Montagnani, and Z. Layrisse, “Preeclampsia: a multifactorial disease resulting from the interaction of the feto-maternal HLA genotype and HCMV infection,” The American Journal of Reproductive Immunology, vol. 48, no. 3, pp. 176–183, 2002. View at Publisher · View at Google Scholar · View at Scopus
  101. F. Xie, Y. Hu, L. A. Magee et al., “An association between cytomegalovirus infection and pre-eclampsia: a casecontrol study and data synthesis,” Acta Obstetricia et Gynecologica Scandinavica, vol. 89, no. 9, pp. 1162–1167, 2010. View at Publisher · View at Google Scholar · View at Scopus